Temporal partitioning and the potential for avoidance behaviour within South African carnivore communities

Abstract Carnivora occupy many ecological niches fundamental to ecosystem functioning. Within this diverse order, carnivore species compete to establish dominance, ensure survival and maintain fitness. Subordinate carnivores must, therefore, adapt their behaviour to coexist with dominant species. One such strategy is the partitioning of temporal activity patterns. We aim to determine interspecific avoidance patterns among sympatric carnivores by examining coexistence along a temporal axis. We compared the temporal activity patterns of 13 carnivore species using multi‐seasonal camera trapping data from four protected areas across South Africa: Associated Private Nature Reserves, Madikwe Game Reserve, Mountain Zebra National Park and Tswalu Kalahari Reserve. Interspecific coefficients of overlap in diel and core activity periods were calculated over the study period and during the wet and dry seasons. Furthermore, interspecific spatiotemporal behaviour was examined using time‐to‐event analyses. Our results showed that complete avoidance of diel activity patterns was rare among South African carnivore species. Most species were predominantly nocturnal and, therefore, diel activity overlap was high, whereas core activity overlap was significantly lower (p < .001). Diel activity overlap was significantly lower during the dry than wet seasons (p = .045). Lastly, evidence of spatiotemporal aggregation revolved around scavenging species. We show the importance of seasonality in the temporal avoidance behaviours of South African carnivores while highlighting the need for fine‐scaled behavioural analyses. Overall, we show that the daily activity patterns of most subordinate South African carnivore species are not influenced by top‐down forces in the form of competitional suppression and risk exerted by dominant species. If avoidance is required, it is more likely to manifest as fine‐scaled avoidance of core activity periods. We suggest that the focus on core activity periods might be a more suitable tool for interspecific temporal partitioning research.


| INTRODUC TI ON
Carnivores (species of the order Carnivora) are integral to an ecosystem's trophic structure and are, therefore, vital to ecosystem functioning (Elmhagen et al., 2010;Estes et al., 2011;Hoeks et al., 2020). They occupy various levels within this trophic hierarchy, and many species fill the role of both predator and prey (Palomares & Caro, 1999). Sympatric carnivores, therefore, likely experience different degrees of competition and risk, from indirect exploitation of limited resources to interference competition that involves direct antagonistic interactions, such as kleptoparasitism, depredation and territorial killings (Caro & Stoner, 2003;Linnell & Strand, 2000;Palomares & Caro, 1999). Outcomes of interspecific competition among carnivores are usually dictated by body size, predatory behaviour, morphological adaptations, age structure, social organisation and species diversity within the region (Donadio & Buskirk, 2006;Lehmann et al., 2017;Linnell & Strand, 2000). Even though interspecific avoidance behaviour is adaptive and manifested over evolutionary timescales, subordinate carnivores must often adjust their behaviour to ensure coexistence with more dominant carnivores due to population-wide changes of, for instance, demographics and sex ratios (Kronfeld-Schor & Dayan, 2003;Lehmann et al., 2017;Lima & Dill, 1990;Linnell & Strand, 2000;Trinkel & Kastberger, 2005).
Avoidance behaviour constitutes many dimensional considerations related to niche theory, ranging from spatial, temporal and diet partitioning, to reliance on reactive or predictive decision making in response to various forms of interspecific competition and risk (Broekhuis et al., 2013;Carothers & Jaksic, 1984;Hayward & Kerley, 2008;Linnell & Strand, 2000). Spatial partitioning may force subordinate species to occupy areas with unfavourable resource availability (Ritchie & Johnson, 2009). In response, these species may resist exclusion from favourable habitat by being active at different times of the day, reducing the likelihood of encounters with the dominant species (Swanson et al., 2014).
Temporal avoidance behaviour is a form of resource partitioning whereby animal species, constrained by morphological characteristics and adaptations, are active at different periods of the 24-h day to reduce the risk posed by species that occupy higher levels of the dominance hierarchy (Schoener, 1974; see review by Bennie et al., 2014;Hayward & Slotow, 2009;Kronfeld-Schor & Dayan, 2003). Temporal partitioning is, thus, a behavioural adaptation that species could employ to coexist with other species deemed a threat to their survival or fitness (Carothers & Jaksic, 1984).
In this study, we used data from Snapshot Safari's extensive camera-trapping surveys within four South African protected areas (Pardo et al., 2021) to assess temporal partitioning as a strategy for interspecific avoidance behaviour among carnivore species.
Examining multiple carnivore communities from environmentally diverse regions will allow for a better understanding of the many different species' temporal behaviours.
Due to their opportunistic predatory behaviour, felids (e.g. lions Panthera leo, leopards Panthera pardus and caracals Caracal caracal) are responsible for most intraguild killings (Curveira-Santos et al., 2022;Donadio & Buskirk, 2006). We, thus, hypothesise that subordinate carnivore species will more likely avoid felids, which could potentially be a greater risk for their survival than the other species. Leopards have been observed killing carnivore species as small as genets (Curveira-Santos et al., 2022). From this, we predict that subordinate carnivore species of all body sizes will show signs of avoiding leopards. Interspecific antagonism and killing are not only limited to large carnivores but are also observed among mesopredators. For example, caracals have been shown to kill smaller carnivore species such as African wildcats Felis silvestris lybica and mongooses (Curveira-Santos et al., 2022). Avoidance behaviour is, therefore, predicted to also manifest among the smaller carnivore species.
Pronounced seasonal variations in environmental characteristics are experienced within South Africa due to its higher latitudes (Daan & Aschoff, 1975). These differences range from unimodal rainfall seasons that result in clear seasonal differences in vegetation quality (i.e. wet and dry seasons), to changes in the availability of resources that could affect the behaviour of carnivores. For example, diet overlap between bat-eared foxes Otocyon megalotis and aardwolves Proteles cristata is likely to occur only during the colder months of the year, when aardwolves shift a considerable portion of their diet to Hodotermes termites due to less availability of the preferred Trinervitermes termites (Kamler et al., 2013;Williams et al., 1997).
As a result, the two species may compete during winter. In addition, Kamler et al. (2017) showed that bat-eared foxes have significantly larger group sizes during the dry seasons in the Northern Cape, South Africa. This was proposed as a possible response of bat-eared foxes to increased temporal overlap with black-backed jackals Lupulella mesomelas in the reserve during the dry season (Kamler et al., 2017). Périquet et al. (2021) showed that seasonality plays an important role in the facilitative and competitional relationship between lions and spotted hyaenas Crocuta crocuta, as resource availability varies between the wet and dry seasons, and spotted hyaenas are more likely to actively hunt prey during the dry season, making them less dependent on scavenging lion kills. Ultimately, we predict that indications of avoidance behaviours among many carnivore species will differ between the wet and dry seasons.

T A X O N O M Y C L A S S I F I C A T I O N
Behavioural ecology, Community ecology temporal overlap values when diel activity is compared. However, temporal avoidance may still be used to coexist, which necessitates finer-scaled temporal comparisons of activity. Therefore, we predict that interspecific temporal avoidance behaviour among the carnivores in this study will more likely manifest as finer-scaled asynchronization of their core activity periods than complete avoidance throughout the 24-h diel period.

| Study areas
Snapshot Safari's camera trapping data from four protected areas across South Africa were included in this study (Pardo et al., 2021;Figure

| Analysis
We only included Carnivora species with at least 20 independent detections within a specific protected area in the analyses. Photocaptures were rendered independent by limiting the time interval between subsequent photo-captures of the same species at a F I G U R E 1 Snapshot Safari's camera trapping networks in the four South African protected areas. Each protected area's fenced borders are represented by solid lines, whereas unfenced borders are represented by stippled lines. The dots in each protected area indicate the locations of camera traps. specific camera station to a minimum of 60 min, reducing the possibility of pseudoreplication (Niedballa et al., 2019).

| Interspecific activity overlap
We compared the daily activity patterns of species populations derived from kernel density estimates within the specific protected areas. This was done by calculating the coefficient of overlap (Δ) and the associated 95% smoothed bootstrapped confidence intervals with 10,000 resamples using the overlap package (Meredith & Ridout, 2021;Ridout & Linkie, 2009) in R (v4.0.3; R Core Team, 2021).
The coefficient of overlap is a proportional value representing the possible similarity in species' diel activity patterns and ranges from 0 to 1, indicating completely different and identical activity patterns, respectively. According to Meredith and Ridout (2021), when at least one species in a pair obtained <50 photo-captures, the overlap estimator Δ 1 was calculated, and when both species obtained more than 50 photo-captures, Δ 4 was calculated.
We also calculated the core activity periods (50% core isopleths) and their overlap between species using the circular package (Agostinelli & Lund, 2022) in R and the highest species-specific bandwidth estimation within each species-pair. An appropriate bandwidth value for each species was calculated with a maximum moment, kmax = 3.
To determine whether there are differences between diel and core activity overlaps, we compared the collective diel activity overlap and core activity overlap values for all the carnivore species-pairs using paired Wilcoxon tests (α = 0.05) with the wilcox.test function in R. Using the same test, we determined the seasonal differences in overlap values by comparing the wet and dry season's collective diel activity overlaps, as well as the two seasons' collective core activity overlaps.
The two separated sections of TKR, Lekgaba (lions present) and Korannaberg (lions absent) present a unique opportunity where the behaviour of a mammal species can be compared within the same region with similar environmental characteristics, but where lions are present and absent. Therefore, to test the effect of lion presence on the daily activity patterns of carnivore species in TKR, we used similar analyses as described above to compare each carnivore species' diel activity pattern separately between the Lekgaba (lions present) and Korannaberg (lions absent) sections of TKR.

| Fine-scaled spatiotemporal behaviour between species
We performed a time-to-event analysis, derived from Karanth et al. (2017) and Watabe et al. (2022), to determine spatiotemporal avoidance or aggregation between carnivore species. In this context, the spatiotemporal dimension refers to differences in temporal use within a shared space. The analysis entailed extracting the time period from each photo-capture of a specific species (reference species) to the nearest single photo-capture, before or after, of the comparing species (proximate species) at shared camera trapping stations. A maximum of 7 days before and after each reference detection was used to include proximate detections, as this allowed for enough comparisons among species while still likely maintaining biological relevance. To increase reliability, we only included speciespairs with at least 20 total comparisons across all camera stations within 7 days before and after the reference detections. We then calculated the observed median of all time intervals between reference and proximate detections within the 7-day relevance period.
We then applied a randomisation process to each photo-capture of the proximate species. This entailed randomly selecting a camera TA B L E 1 Characteristics and deployment data of the Snapshot Safari camera trap networks in four South African protected areas: Associated Private Nature Reserves (APNR), Madikwe Game Reserve (MGR), Mountain Zebra National Park (MZNP) and Tswalu Kalahari Reserve (TKR). station, date and time from the original dataset for the specific proximate species, thereby preserving biological relevance in activity period preferences. This was repeated 1000 times to generate 1000 randomised datasets against which the reference species detections were compared in the time-to-event analysis. The median of the minimum time between proximate and reference detections for each 1000 randomised datasets was then calculated and plotted as a density distribution of medians. Similar to standard permutation tests, we calculated a proportional value (p-value) as p = n ∕ N, where n is the number of randomised medians greater than the observed median and N is the total number of randomised medians for the specific species-pair. A two-tailed significance level (α = 0.05) was considered, where a p > .975 indicated a significant possibility of spatiotemporal aggregation and p < .025 indicated a significant possibility of avoidance behaviour.

| RE SULTS
Within each of the sites, six species obtained 20 or more independent photo-captures (Table 2). Therefore, we were able to look at a total of 13 species across the four protected areas, with approximately half White-tailed mongoose Ichneumia albicauda 2 2 0 being mesocarnivores. The body sizes of these species range from the largest predator, lions, to the small mesopredator, African wildcats.

| Interspecific overlap in temporal activity patterns
The majority of the species assessed within the four protected areas were primarily nocturnal ( Figure 2 Table A1). Overall, the overlap of the carnivore species' core activity periods (Δ core ) was significantly lower (V = 1711, p < .001) than the overlap of their 24-h diel activity patterns (Δ diel ).
More specifically, APNR's African wild dogs showed moderate to low temporal overlap with most other carnivore species. This was especially noticeable when core activity periods were compared ( Figure 3; Table A1 (Figures 3 and 4; Table A1). In addition, the majority (13 of 15) of carnivore species-pairs assessed in TKR had a moderate or higher Δ core ; only brown hyaenas paired with aardwolves and African wildcats had a low Δ core . Lastly, TKR's Cape foxes had very high Δ diel and Δ core with the reserve's bat-eared foxes and blackbacked jackals.

| Seasonality in interspecific temporal overlap
Most of the species-pairs assessed within the protected areas had very high Δ diel during the wet seasons and high Δ diel during the dry seasons ( Figures 5 and 6; Table A2). Although marginal, this resulted in a significant difference in Δ diel between the two seasons (V = 173.5, p = .045). However, with the test statistic again being marginal, there was no significant difference in Δ core between the two seasons (V = 170.5, p = .058).
All of the carnivore species assessed within APNR had high to very high Δ diel during both seasons ( Figure 5; Table A2). Furthermore, these species all had moderate Δ core during the wet seasons, except for African civets paired with leopards which had a high Δ core . During the dry seasons, the Δ core of APNR's lions paired with spotted hyaenas, and African civets decreased to a very low level, whereas APNR's African civets maintained a high Δ core with the reserves' leopards.
Most species assessed within MGR had high Δ diel during the wet and dry seasons, with only spotted hyaenas paired with brown hyaenas having a very high Δ diel ( Figure 5; Table A2). Furthermore, all of MGR's species assessed during both seasons experienced a decline in Δ core during the dry season. Most notably, the Δ core of brown hyaenas and spotted hyaenas decreased from a moderate Δ core during the wet season to a low Δ core during the dry season.
MGR's black-backed jackals had high Δ diel with spotted hyaenas during both seasons, but low and very low Δ core during the wet and dry seasons, respectively.
All of the species that were assessed during MZNP's wet and dry seasons had high or very high Δ diel ( Figure 5; Table A2). Most of these species also had moderate to high Δ core . However, bat-eared foxes paired with brown hyaenas in MZNP had very low Δ core during both seasons, as did bat-eared foxes paired with aardwolves, but only during the dry seasons ( Figure 5; Table A2). The most noticeable seasonal difference in Δ core within MZNP was between aardwolves and bat-eared foxes, with 87% less overlap during the dry compared to wet seasons.

F I G U R E 2 (Continued)
All of TKR's species that were assessed during the wet and dry seasons had very high Δ diel ( Figure 5; Table A2). Most of these species also had moderate or higher Δ core , with low Δ core observed between TKR's brown hyaenas and bat-eared foxes during both seasons, brown hyaenas and Cape foxes during the wet season, and between the two fox species during the dry season. Cape foxes and bat-eared foxes had very similar activity patterns during the wet seasons, with a marked decrease during the dry seasons, especially in Δ core . In contrast, bat-eared foxes and black-backed jackals had substantially more overlap during the dry than wet seasons ( Figure 5; Table A2).

| Spatiotemporal behaviour
Only 11 species-pairs across all four protected areas obtained enough (≥20) proximate photo-captures within 7 days of the refer- or segregation, the majority had p-values closer to indications of aggregation (p > .5) than segregation (p < .5; Figure 7).

| DISCUSS ION
In this study, we compared the activity patterns of South African Carnivora species to investigate temporal partitioning as a potential avoidance mechanism to reduce encounters with more dominant carnivores. However, most species-pairs (63%) across all combinations and sites in this study showed no clear indications of using temporal avoidance behaviour as a strategy to coexist with a potential risk-associated, dominant species. A trade-off exists in subordinate carnivores between resource acquisition and risk associated with sympatric predators (Linnell & Strand, 2000), with the former likely outweighing the latter in most cases in this study. This is a viewpoint shared by many previous studies on African carnivores, in which hunting success is said to be prioritised over the possibility of encountering dominant predators (see Balme, Pitman, et al., 2017;Cozzi et al., 2012;Miller et al., 2018;Mugerwa et al., 2017;Müller et al., 2022).  et al. (2013) in showing that the activity patterns of bat-eared foxes are not influenced by a common risk-associated species such as black-backed jackals. Furthermore, black-backed jackals pose a significant threat to Cape foxes and will kill them in territorial defence, leading to the suppression of Cape fox populations (Kamler et al., 2013). Conversely, TKR's Cape foxes showed no evidence of temporally avoiding black-backed jackals, which contradicts previous findings (Edwards et al., 2015;Kamler et al., 2012). Bateared foxes and Cape foxes have little dietary overlap and do not recognise each other as a noticeable antagonistic threat (Kamler et al., 2012). Therefore, avoidance behaviour between the two fox species is highly unlikely and was not observed in this study as both fox species had very similar daily activity patterns. In addition, our findings support the idea that leopards use strategies other than temporal partitioning to coexist with other large carnivores (Miller et al., 2018). One such method is the characteristic caching behaviour of leopards, in which they hoist prey carcasses into trees to avoid kleptoparasitic losses, lending support to the kleptoparasitism-avoidance hypothesis MacDonald, 1976). Furthermore, this study supports Ramesh et al. (2017), who showed that smaller carnivores rarely use temporal partitioning to avoid large carnivores.

Nocturnality in many large carnivores is attributed to in
Notably, the presence of lions within the Lekgaba section of TKR did not affect the activity patterns of brown hyaenas, black-backed jackals and bat-eared foxes. We suggest two possible explanations: (1) Mesocarnivore suppression in terms of temporal behaviour is comparable among lions and other carnivore species that fill the role of apex predators when lions are removed from an ecosystem (e.g. Korannaberg's African wild dogs), or (2)

F I G U R E 7
Relative spatiotemporal behaviour of carnivore species within the four South African protected areas. The first-mentioned species are the reference species within the pair. The shaded density distribution represents 1000 randomised medians of time between reference and proximate detections, whereas the vertical stippled line represents the median observed time between reference and proximate detections. The p-value shows the proportional number of randomised medians greater than the observed median and n represents the total number of proximate detections obtained within the 7-day period before and after the reference detections.
of site-specific carnivore densities is also important because low densities result in the rarity of encounters, which may make temporal avoidance negligible (Mills, 2015;Müller et al., 2022;Romero-Muñoz et al., 2010). As the densities of the species increase, so will the number of encounters between them (Creel et al., 2001).
This may have been the case in the significant spatiotemporal aggregation between MZNP's aardwolves and black-backed jackals.
Documented cases of aardwolves being attacked and killed by blackbacked jackals are lacking (Curveira-Santos et al., 2022), and there is a negligible overlap in their diets (Klare et al., 2010). Therefore, it can only be assumed that this aggregation was due to factors other than interspecific attraction, such as the high detection frequency of black-backed jackals or an attraction to similar habitat with high productivity. However, we recommend that future research should aim to refine the time-to-event method of interspecific spatiotemporal analyses by examining the effect of detection frequencies and population densities on outcomes, the effect of multiple species occurring after a reference detection, and the chosen maximum time between reference and proximate detections as longer periods may present issues of randomisation. These are potential limitations to obtaining reliable results from which robust inferences could be made.
The potential for competition between specific carnivore species is also important when determining possible temporal avoidance behaviour (Caro & Stoner, 2003). Even though competition between most sympatric carnivore species is theoretically acknowledged, it should be empirically confirmed through direct observations of antagonistic behaviour. For instance, inter-species killings have been documented (Palomares & Caro, 1999), but these events may be rare enough to be considered negligible. We predicted that subordinate carnivore species would avoid felids such as lions and leopards more than other carnivores due to their opportunistic predatory behaviour, which leads to them being responsible for most intraguild killings (Curveira-Santos et al., 2022;Donadio & Buskirk, 2006). However, our results do not clearly distinguish the prevalence of avoidance behaviour between felids and other carnivore species such as hyaenas and black-backed jackals and, therefore, does not provide clear support to this hypothesis. In addition, the study does not support the prediction that subordinate carnivores of all body sizes (e.g. APNR's African civets, and MGR's

F I G U R E 7 (Continued)
brown hyaenas, black-backed jackals and African wildcats) will show signs of avoiding leopards temporally. Lions, however, appear to affect the core activity periods of many subordinate carnivore species and, therefore, this study suggests that subordinate carnivores will be more inclined to avoid the core activity periods of lion prides than solitary leopards.
Some species-pairs displayed clear potential for temporal avoidance behaviour. This mainly revolved around the crepuscularity of the APNR's African wild dogs, and the cathemeral behaviour of MZNP's caracals. African wild dogs are vulnerable to interference competition from larger carnivores such as spotted hyaenas and, in particular, lions (Creel & Creel, 1996). As a result, African wild dogs may have undergone forced evolutionary adaptations for activity preferences during crepuscular periods (Swanson et al., 2014).
It should be noted that non-overlapping activity patterns do not necessarily indicate avoidance behaviour, but that the potential for avoidance behaviour exists.
Most species-pairs that displayed possible temporal avoidance behaviour in this study were predominantly nocturnal and, thus, likely rely on finer-scaled temporal partitioning via adaptations to activity peaks and core activity periods to facilitate coexistence. This was evident in our findings as core activity overlap was significantly lower compared to diel activity overlap in most species-pairs. Our findings, therefore, satisfy the prediction that interspecific temporal avoidance behaviour among South African carnivores will more likely be expressed as finer-scaled asynchronization of their core activity periods than complete avoidance throughout the 24-h diel period. This allows species to remain active when hunting success is greatest, while reducing the risk of encounters with dominant species, which may be less costly to manage than large-scaled avoidance (Broekhuis et al., 2013).
For example, brown hyaenas are scavenging specialists and are facilitated by the presence of larger carnivores, such as lions, as they benefit from eating the remains of their kills (Mills, 2015).
However, our findings show that brown hyaenas use fine-scaled partitioning of core activity periods to avoid direct interactions with lions. This finding is supported by Mills and Mills (1982) and Bashant et al. (2020). We also found evidence of fine-scaled avoidance behaviour in two facultative scavengers; MGR's black-backed jackals peaked in activity before and after spotted hyaena activity peaks. This study recommends that future research on temporal avoidance behaviour should focus on finer-scaled avoidance of, for example, core activity periods.
Seasonal considerations are also important when comparing the daily activity patterns of carnivore species (Vilella et al., 2020).
We observed a relatively common trend in which the temporal overlap between species was noticeably lower during the dry seasons compared to the wet seasons. This trend has also been reported by Finnegan et al. (2021)

ACK N O WLE D G E M ENTS
The Snapshot Safari SA project is funded and supported by the South African National Biodiversity Institute, the Foundational Biodiversity Information Programme (Grant no. FBIP170720256205) and the National Research Foundation. We thank the managers and land owners of the various properties for permission to do the work. We also thank the numerous people who assisted in servicing the project's camera traps. This study was approved by the Nelson Mandela University Animal Ethics Committee (A19-SCI-NRM-001).

CO N FLI C T O F I NTE R E S T S TATE M E NT
There are no conflicts of interest to declare.

TA B L E A 2
The temporal activity overlaps of carnivore species during the wet and dry seasons within South Africa's Associated Private Nature Reserves (APNR), Madikwe Game Reserve (MGR), Mountain Zebra National Park (MZNP) and Tswalu Kalahari Reserve (TKR).